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OCR for page 245
Pesticide Resistance: Strategies and Tactics for Management.
1986. National Academy Press, Washington, D.C.
Response of Plant
Pathogens to Fungicides
M. S. WOLFE and I. A. BARRETT
Genetic variationforfungicide resistance must occur if a pathogen
is to respond to fungicide use. The rate of pathogen response depends
on a complex interaction between the exposure of the pathogen to
the fungicide, the biology of the pathogen, and the environment. An
example of this interaction is the response of the barley mildew
pathogen Erysiphe graminis f. sp. hordei to the widespread use of
triazole fungicides in the United Kingdom, which also illustrates the
interaction of fungicide resistance and host pathogenicity.
The current strategies of fungicide use tend to exacerbate the
problem of restraining pathogen response. Other strategies, based
on different forms of diversification, may be helpful in practice, at
least under western European conditions. Experiments were con-
ducted with fungicide treatments of the seed of single components
of mixtures of host varieties having different resistance genes. On
the farm this system can give good disease control and predictably
high yields at low cost. Durability is not predictable, except that it
is likely to be better than with current strategies, with the additional
benefit of restricting the response of the pathogen to resistant hosts.
INTRODUCTION
This paper is an amalgam of first principles and practical experience gleaned
largely from research on the control of Erysiphe graminis f. sp. hordei on
barley. The use of fungicides changes the environment of the pathogen, and
to understand its response requires a knowledge of how such changes affect
selective differences between different genotypes in the population. Only
245
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246 POPULATION BIOLOGY OF PESTICIDE RESISTANCE
then can a way that is acceptable biologically and for practical crop production
be developed to modify the response.
FUNGICIDE USE
The Attraction of Fungicides
Why are fungicides used? Broadly, there are three reasons. The first is to
control disease during crop development. Among field crops the view is
encouraged that a particular species or variety is susceptible and thus losing
yield to a disease, that the plant breeders have failed to deal with the problem,
and that fungicides will provide the answer. The perception of susceptibility
in commercial production, however, is based on an assessment relative to
complete absence of disease. Truly susceptible host lines are eliminated
during the breeding process and are rarely seen in agriculture; those that are
deemed susceptible but remain in cultivation often have yields of only 20
percent (or less) below their potential maximum. Fungicides are used ex-
tensively to remove this limitation so as to achieve the "ideal" of a disease-
free crop.
Initially at least, fungicides remove these restraints consistently and reliably
because the recommended dose rates are determined from field trials with
adequate pathogen inoculum applied to the currently most susceptible com-
mercial varieties. For the farmer the fungicide controls the disease perfectly
because his varieties, on average, will be less susceptible than those used in
manufacturers' trials, and his farm conditions will tend to be less favorable
for disease development.
For these same reasons many fungicide applications expose the pathogen
to a fungicide for no economic return, but the psychological impact of
the clean crop more than offsets this hidden factor. A similar psychological
problem arises from using fungicides to eliminate blemishes completely
from produce for direct consumption. Perfect produce has become the
norm for the marketplace even though it may not be essential, productivity
is not improved, and exposure of pathogens to fungicides is maximized.
The demands for clean crops and perfect produce mean that fungicides
are used increasingly as prophylactic treatments known to cereal farmers
in eastern England as the sleep-easy factor despite the consequences.
The second reason for the use of fungicides is to improve the storage
of produce. Perfect control of storage diseases increases the size and
duration of the market available for the product. Thus, the marketplace
again encourages widespread use of fungicides, particularly since plant
breeders do little or nothing directly to breed for resistance to storage
diseases.
Third, with fungicides growers can increase production of a particular crop
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RESPONSE OF PLANT PATHOGENS TO FUNGICIDES
247
and reduce their dependence on conventional controls of crop rotation and
sanitation. Moving away from the costs and constraints of conventional
controls is double-edged: the fungicide usage per unit area is increased, as
is the total area of the crop and the size of the potential medium for the target
pathogen. The increased potential for the crop provided by the fungicide is
often so dramatic initially that some manufacturers suggest that breeders need
no longer breed for host resistance. Any decrease in attention to inherent
host resistance, however, is almost certain to exacerbate and accelerate se-
lection of fungicide resistance, simply because pathogen survival is made
easier.
Fungicide Application and Type
The area treated with a fungicide contains the effective treated area, defined
as the proportion of the crop at any one time in which the fungicide level is
higher than the threshold of control of the common fungicide-sensitive gen-
otypes of the pathogen. For example, if equal amounts of two different
fungicides are applied to a crop but one is more systemic and persistent than
the other, the effective treated area of the first will be greater. Disease control
will be greater, but so will the advantage accruing to resistant genotypes of
the pathogen.
Fungicides may be formulated for use as seed treatments, or as foliar
sprays, or both. Seed treatments are potentially more effective because they
may control the pathogen when the population is at its smallest and thus
delay epidemic development, particularly if the compound is systemic and
persistent. The corollary is that the pathogen population has a longer exposure
to the treatment. If a fungicide is formulated both as a seed treatment and
as a foliar spray and the compound is used widely and sequentially in the
two forms, the effective treated area and the advantage to resistant genotypes
are greatly increased.
Broad-spectrum fungicides, as opposed to selective fungicides, may com-
pound the problem if they remove competitors or hyperparasites that would
assist the activity of a selective fungicide. Thus, the greatest potential for
fungicide resistance comes from the large-scale prophylactic use of a broad-
spectrum, systemic, and persistent material applied to the seed and then to
the foliage. The fungicide initially controls the disease dramatically, and it
is easily sold to farmers who are mostly risk-averse. The alternative of a
nonpersistent, selective foliar spray, applied only when the disease level
passes a defined threshold, is risky and demands accurate monitoring, fore-
casting, and assessment of yield loss, but it reduces the time over which the
pathogen is exposed to the fungicide and thus reduces the probability of
resistance evolving.
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248
POPULATION BIOLOGY OF PESTICIDE RESISTANCE
PATHOGEN RESPONSE
A Priori Considerations
Any response to fungicide use depends, first, on whether genetic mech-
anisms exist to reduce or eliminate the effects of the fungicide. The mech-
anisms may occur at low frequencies before the fungicide is introduced, they
may occur as mutations, or both. The rate at which the pathogen responds
then depends on the interaction between the mechanisms available and their
genetic control, the use of the fungicide, the biology of the organism, and
the environment.
One major factor is whether the organism is diploid or haploid in the
asexual stage. If haploid then any mutation to fungicide resistance is im-
mediately expressed, and the frequency of the mutant will be influenced by
its effect on fitness. With a diploid organism the situation is more complex;
there may be a cryptically high frequency of resistance, depending on the
fitness of the heterozygotes and resistant homozygotes relative to the wild
type, in the presence and absence of the fungicide (Barrett, in press).
The rate of response of a pathogen also depends on its breeding system,
principally on whether there is an obligate sexual or parasexual sequence in
the life cycle. An effective sexual stage allows for more rapid formation of
novel combinations of appropriate characters through recombination, which
may increase the fitness of the resistant pathogen genotypes. With no sexual
stage, linkage disequilibrium between resistance and other characters is likely
to persist, which may limit or delay adaptation of the pathogen to the treated
host population.
The spread of fungicide resistance depends on the distribution of propa-
gules: populations of foliar pathogens with airborne spores will respond more
rapidly than soil-borne pathogens. Finally, the ability of a pathogen to respond
to fungicidal control depends on its ability to cope with other environmental
stresses. An organism at the limits of its ability to survive in a particular
environment will be less able to respond to an extra stress. For example, the
greater the level of disease resistance and diversity in the host crop the less
likely it will be for a pathogen to develop and spread resistance to a fungicide.
Dynamics
Wolfe (1982) summarized the interaction of selection for resistance and
for other characters. Whether fungicide resistance increases in a population
is determined by the size of the effective treated and untreated areas and the
fitness of the forms of the pathogen with different sensitivities to the fungicide
on each of these areas. There will tend to be large differences in fitness on
the treated crop and smaller differences on the untreated. If the differences
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RESPONSE OF PLANT PATHOGENS TO FUNGICIDES
249
on the untreated crop area are small, then a small area of treated crop may
allow resistant forms of the pathogen to predominate in the population as a
whole. If the fitness differences on the untreated crop are large, then fun-
gicide-resistant forms of the pathogen may not become apparent until there
is a large treated area. The overall fitness of sensitive and resistant forms of
the pathogen, therefore, depend on the area of fungicide treatment. Growth
rate differences between isolates measured in the laboratory may have little
relevance to the fate of those isolates in the field.
Monitoring the range of forms of a pathogen with reduced sensitivity to
a fungicide is difficult. The phenotypes isolated first may not be the ones
that eventually become common, because recombination and selection may
change the expression of resistance during its spread. Indeed, if selection is
maintained it is never possible to predict when the response will cease. In
the example of barley mildew adapting to the use of ethirimol, Brent et al.
(1982) noted a shift to an apparent equilibrium between sensitivity and re-
sistance in the pathogen population. In this case, however, selection for
resistance declined when ethirimol was replaced by other fungicides and
more resistant varieties: the apparent equilibrium may have been a temporary
peak associated with maximum use of the fungicide.
AN EXAMPLE
The worst case in terms of selection for resistance is where a systemic,
persistent, and broad-spectrum fungicide is applied sequentially on the major
part of the crop area to control a well-adapted foliar pathogen that is efficiently
dispersed by airborne spores and has an effective sexual stage. Among field
crops this combination of characters is exemplified by the use of triazole
fungicides to control barley mildew in western Europe.
Shortly after introduction of these fungicides into commercial use in the
United Kingdom, the first isolates with some resistance were identified in
small populations surviving on treated crops (Fletcher and Wolfe, 1981~.
From 1981 the air spore was monitored continuously (Wolfe et al., 1984a)
by means of a simple spore trap mounted on a car roof (Wolfe et al., 1981;
Limpert and Schwarzbach, 19811. The numbers of colonies that incubated
on seedlings with different doses of the fungicide increased annually relative
to the numbers on untreated seedlings. The early surveys could not always
detect isolates with fungicide resistance in the small populations on treated
crops; by 1984, however, such isolates were detected easily on untreated
crops.
The increase in frequency of the less-sensitive phenotypes showed two
interesting characteristics. The first was that the rate of increase varied during
the year. This variation was repeated between years, which suggested that
during the spring, following seed treatment and early foliar sprays, there
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250
POPULATION BIOLOGY OF PESTICIDE RESISTANCE
TABLE 1 Mean Pathogenicity (Pathog.) on Six Differential Barley Hosts of
Powdery Mildew Isolates with Different Levels of Sensitivity to Tr~adimenol
Obtained from Untreated and Treated Seedlings in a Car Spore Trap in East
Anglia, 1981-1983
Seedling 1981 1982 1983
Source EDso Pathog. ED50 Pathog. ED50 Pathog.
Untreated 0.028 32 0.060 40 0.080 35
0.025a 0.045 27 0.080 35 0.093 35
0.125a 0.085 7 0.093 25 0.108 35
aGrown from seed treated at 0.025 or 0.125 g a.i./kg.
SOURCE: Wolfe (in press [a]).
was rapid selection toward resistance. During the summer the response slack-
ened or reversed, presumably following dissipation of the fungicide. At the
beginning of autumn, however, frequency sharply increased, probably due
partly to release of ascospores from cleistothecia formed at the time of
relatively high frequencies of resistance at the end of spring and partly to
the influence of emerging crops of treated winter barley. During autumn and
winter the frequency of resistant forms again declined.
In pathogen populations on individual field crops of treated winter barley,
the frequency of the most resistant forms was high on seedlings in the autumn
because of the selection imposed by the high concentration of fungicide in
the seedling leaf tissue (Wolfe et al., 1984a). As the plants grew and the
concentration decreased, the frequency of these forms decreased and forms
with intermediate resistance became predominant. On the untreated crops
sensitive forms were initially predominant, but, again, forms with interme-
diate resistance eventually became more common, presumably due to spores
migrating from other crops, most of which would have been treated at some
stage.
The second major feature of interest was the relationship between resistance
and pathogenicity. During the early stages of the overall increase in resis-
tance, the more resistant forms of the pathogen were less pathogenic on the
range of host varieties in common use at the time (Table 11. In subsequent
seasons, however, pathogenicity of the sensitive fraction remained constant,
but the resistant fraction gradually increased to the same level.
The increase in pathogenicity in the resistant part of the population occurred
earlier for some characters than for others. For example, resistance increased
first in Scotland and northern England in populations having a high frequency
of pathogenicity for varieties with the Mla6 resistance gene. This created
linkage disequilibrium, and isolates having these characters rapidly became
common throughout the United Kingdom. The potential value of Mla6 was
thus diminished in areas where it was not in current use. Simultaneous with
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RESPONSE OF PLANT PATHOGENS TO FUNGICIDES
251
these changes the resistant variety Triumph became extensively cultivated
and increasingly susceptible. Triazole fungicides thus became widely used
on Triumph; isolates resistant to triazoles are now commonly pathogenic on
Mla6 or Triumph or both.
As fungicide resistance in the pathogen population increases, there may
be loss of disease control and a reduction in the yield advantage expected
from treatment. Initially such effects have a patchy distribution. Not all
resistant isolates will be associated with poor fungicide performance and,
conversely, not all poor fungicide performance will result from the oc-
currence of fungicide-resistant isolates. Inevitably, during the first seasons
of using a new fungicide, there will be some instances of poor control
due to incorrect application and other environmental problems. This small
proportion will fluctuate from season to season; a real deterioration in
fungicide performance will be signalled by a continuing increase in in-
stances of poor control.
For example, with triazoles and the control of barley mildew, following
the increase in frequency of resistant forms in eastern England, performance
of triazoles both in disease control and in yield benefit rapidly declined (Table
21. The effect was most marked in varieties with the Mlal2 resistance gene;
the yield increase following treatment declined from 25 percent in 1982 (P
< 0.001) to 3 percent in 1984 (not significant), during which time ethirimol-
a different seed treatment that was less widely used gave a consistent yield
advantage of around 10 percent (P < 0.051. A similar yield advantage during
this period was obtained with ethirimol applied to Carnival (Mla6), but there
was no advantage with triazole treatment, probably because of the higher
frequency of resistant isolates carrying pathogenicity for Mla6 compared
~ ~ 1 _ ~ 1 ~
with those pathogenic against Blab;. A more complex ~n~erac~on warn Anise
fungicides was obtained with Triumph and Tasman because of the declining
resistance of the varieties during this same period. Nevertheless, the perfor-
mance of the triazoles declined relative to that of ethirimol.
CONTROLLING THE PATHOGEN RESPONSE
Reducing exposure of the pathogen to the fungicide is the most obvious
way to deter resistance, and this can be helped by making disease forecasting
more precise and educating growers to the problems. Commercial pressures
against such actions, however, may be strong. Reducing the fungicide dose
may or may not delay resistance development. If the dose is reduced to a
level at which some sensitive genotypes survive, there may be some delay;
however, the pathogen may cause unacceptable yield loss. On the other hand
any delay caused by an increased dose is likely to be followed by emergence
of highly resistant strains of the pathogen. Other changes in the formulation
of the compound or inefficiency of application may also alter the fitness
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252
POPULATION BIOLOGY OF PESTICIDE RESISTANCE
TABLE 2 Yield (t/ha) of Spring Barley Varieties with Different Mildew
Resistance Genes, Untreated or Treated with Ethir~mol or Tr~adimenol,
1982-1984
Variety Year Untreated Ethir~mol-trt. Tr~adimenol-trt.
Ml al2
Egmont 1982 5.01 5.49 6.25
ref. 100 110 125
Patty 1983 3.51 3.90 4.12
ref. 100 111 114
Patty 1984 6.90 7.46 7.13
ref. 100 108 103
Ml ad
Carnival 1982 5.38 5.87 5.64
ref. 100 109 105
Carnival 1983 3.83 4.11 3.84
ref. 100 107 100
Carnival 1984 6.60 7.07 6.53
ref. 100 107 99
Ml flay
Triumph 1982 5.40 5.81
ref. 100 108
Tasman 1983 3.57 3.85 3.70
ref. 100 108 104
Tasman 1984 5.66 6.43 6.05
ref. 100 114 107
NOTE: Standard error for 1982, + 0.11; 1983, + 0.23; 1984, + 0.14.
SOURCE: Wolfe (in press [a]).
differences between sensitive and resistant genotypes and make prediction
difficult.
Reducing the use of a particular compound may need to be accompanied
by other means of limiting pathogen increase, such as diversifying between
fungicides with different modes of action known or thought to be matched
by different pathogen mechanisms. For commercial and technical reasons,
there are considerable constraints to the kinds of action that can be recom-
mended. The current system is the use of mixtures, usually a tank mix of a
systemic and a nonsystemic compound. The data to support this approach
are inconclusive. Adding a nonsystemic material may only temporarily reduce
the absolute population size of the pathogen, while the systemic material
will be more persistent so that after the initial combined action of the fun-
gicides, the pathogen population will be exposed uniformly to the systemic
compound on all plants and thus selected for resistance.
A more effective system, analogous to the use of variety mixtures (Wolfe,
1981), may be to ensure that the compounds eliciting different responses are
applied to adjacent plants. The pathogen must then either adapt to a single
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RESPONSE OF PLANT PATHOGENS TO FUNGICIDES
253
plant or become versatile between plants. Compared with a uniformly treated
stand, there is a greater space between plants receiving the same treatment,
so that increase of the population resistant to that treatment is delayed.
Further, any genotypes with combined resistance to all of the fungicides used
are likely to be less fit on any one plant than the genotype specifically adapted
to the treatment on that plant.
Currently, this approach can be contemplated only for fungicides applied
to seed. Even here treatment on one seed may spread to other seeds treated
differently, and different treatments may vary in their effects on the flow
rate of seed either in a mixing process or in a seed drill. Recent developments
in film coating of seeds may eliminate such problems. Fungicides can be
applied to seed in a carrier material, improving the precision of individual
seed treatment. The material is fixed firmly to the seed, and the flow char-
acteristics of the seed are similar to those of seed treated with other fungicides
(M. D. Tebbit, Nickersons Seed Specialists Ltd., personal communication,
19841. Seeds can also be simultaneously color coded so that intimacy of
mixing can be confirmed.
Future developments in application technology may allow a similar ap-
proach with foliar sprays. For example, ultra-low-volume equipment such
as the electrostatic sprayer raises the possibility of using a square matrix of
containers holding different fungicides, mounted on a frame with a system
of rapid on-off switching so that a fine mosaic of different materials can be
applied.
INTEGRATED DISEASE CONTROL
Unfortunately, much of the discussion on controlling pathogen response
to fungicides makes no reference to the host crop. In the simplest case, with
partially resistant host varieties, the number of treatments and the dose can
be reduced, thereby reducing selection on the pathogen for resistance to the
fungicide and indeed for pathogenicity to the host (Wolfe, 19811.
Sometimes it is more effective to use intimate mixtures of host varieties
with different resistance genes (Jensen, 1952; Wolfe and Barrett, 1980; Wolfe,
1985~. Particularly if diversity between mixtures is maintained in space and
in time, disease control is more consistent and durable than if the components
are used in monoculture. By changing the composition of mixtures as new
varieties become available, both the yield potential and the diversity are
maximized, which suits both the farmer and the plant pathologist.
From 1980 through 1984 four barley varieties with different resistance
genes and the four mixtures of three varieties that can be made from them
were grown in field trials at the Plant Breeding Institute, Cambridge, England
(Wolfe et al., 1984b; Wolfe et al., 19851. Over the trial series the mixtures
outyielded the pure stands by 7 percent (P < 0.0011. The best strategy found
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254
POPULATION BIOLOGY OF PESTICIDE RESISTANCE
TABLE 3 Average Yields (t/ha) and Infection (total percent leaf cover) for
1983 and 1984 of the Three Spring Barley Varieties Carnival, Patty, and
Tasman, Grown as Pure Stands or Mixtures, Untreated or Treated with a
Triazole or Ethirimol at the Normal Field Rate
Yield (t/ha) Infection (total % leaf cover)
.
Pure Rel. Mixed Rel. Pure Rel. Mixed Rel.
Untreated 5.192 100 5.61 ~108 25.7 100 19.3 75
Tr~azole
1/3 S.253a 101 5.622 108 22.62 88 15.2 59
N 5.372 103 5.44 ~105 16.4 64 13.6 53
Ethir~mol
1/3 5.3S3a 103 s.682 109 20.4a 79 10.2 40
N 5.672 109 5.65 ~109 9.7 38 6.3 25
NOTE: The 1/3 treatment of the mixtures is the mean of three mixtures in each, of which only
one component is treated with tr~azole or ethir~mol. The 1/3 treatments of pure stands are calculated
values obtained from the sum of the three pure varieties treated, plus twice their sum untreated,
divided by nine.
aCalculated values.
~SE= +0.16.
2SE = + 0.09.
3SE = + 0.07.
SOURCE: Wolfe (in press [b]).
for the farmer, given the choice of only those four varieties each year, would
have been to grow any one or more of the mixtures. Based on this research
variety mixtures are now grown commercially in the United Kingdom and
Denmark, with generally favorable reports from the farmers involved. A
much larger scale of development is being undertaken in the German Dem-
ocratic Republic, particularly because of the high cost of fungicides in eastern
Europe.
Despite the obvious advantages of the variety mixtures, disease control is
sometimes considered to be inadequate, and some mixtures are treated with
fungicides even though the benefit may be uneconomic. For this reason and
to provide long-term protection for the varieties and the fungicides, exper-
iments have been conducted with fungicide-integrated mixtures (Wolfe, 1981;
Wolfe and Riggs, 19831. The seed of one component of a three-variety
mixture is treated with a fungicide and then mixed with the two untreated
components. Data for two field experiments in 1983 and 1984 are summarized
in Table 3. In these experiments Carnival (Mla6 resistance), Patty (Mlal2),
and Tasman or Triumph (both Mla7 plus MlAb) were grown alone, un-
treated, or treated either with ethirimol or a triazole fungicide. They were
.
also grown as a mixture and in plots where only one component was treated.
All plots were surrounded by guards to reduce interplot interference.
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RESPONSE OF PC4NT PATHOGENS TO FUNGICIDES
255
Although it reduced infection, treating pure stands with triazole did not
increase yields significantly, probably because fungicide resistance increased
during the period. The effect of ethirimol treatment on yield, however, was
highly significant (P < 0.001) and was associated with greater disease con-
trol. Mixing varieties without a fungicide treatment increased yield signifi-
cantly (P < 0.05) and reduced infection, although fungicide treatments of
the mixture had no significant effect.
An interesting but not significant result was that the highest absolute yields
were obtained with the mixtures in which single components had been treated.
For both fungicides the yields of these 1/3 treatments were significantly higher
(P < 0.01) than the equivalent calculated treatment of pure stands. Moreover,
there was considerably less infection on these mixtures than on untreated
mixtures; they were only slightly more infected than the mixtures that received
the conventional fungicide treatment. Comparing the 1/3 treatments of the
mixture with the conventional treatment of the pure stands, the mixture yields
were higher, significantly so for the triazole treatments, and infection levels
were the same.
Thus, for the farmer, using the 1/3 treatment of a variety mixture would
produce a yield as high and a crop as clean as from conventionally treated
pure stands, but at a lower cost. Epidemiologically the fungicide seed treat-
ment protects the crop at the beginning of the epidemic, when variety mixing
is least effective. Later in the growth cycle the crop is protected more by
the varietal heterogeneity, after the fungicide concentration has declined
below the threshold for disease control. Biologically the pathogen is less able
to overcome each variety and fungicide component, and less fungicide is
delivered into the environment. We may also expect to maintain higher yields
with the partly treated mixtures than with the conventionally treated pure
varieties.
CONCLUSION
The response of a pathogen population to fungicide use depends on genetic
variation for resistance being present in the population. When such variation
is present and can be demonstrated, the rate and form of the response will
depend on a complex interaction of the genetic and breeding system and
general biology of the target organism, the range of host varieties in use,
cultivation practices, and the physical environment. The example of powdery
mildew of barley shows how responses can be manipulated using different
forms of crop husbandry. The ability to modify the pathogen response requires
at least an understanding of the genetics and population dynamics of the
pathogen so that the consequences of changes in cultivation practices can be
predicted. Without a reasonable understanding of the population biology of
the pathogen and of the consequences of crop husbandry methods, it is not
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256
POPULATION BIOLOGY OF PESTICIDE RESISTANCE
possible either to understand the responses or to suggest changes in agr~-
cultural practices that might modify the response. The only certain conclusion
is that if variation for resistance exists, and the fungicide is used extensively
and homogeneously, then its effectiveness will soon decline. Unfortunately,
the pathogen may ultimately find a way around any strategy designed to
control it.
ACKNOWLEDGMENT
We wish to acknowledge financial help from ICI Plant Protection Ltd. for
part of the experimental work.
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Representative terms from entire chapter:
population biology
